Exp Brain Res (2013) 226:95–106 DOI 10.1007/s00221-013-3414-7
RESEARCH ARTICLE
Weightlessness alters up/down asymmetries in the perception of self-motion Caty De Saedeleer · Manuel Vidal · Mark Lipshits · Ana Bengoetxea · Ana Maria Cebolla · Alain Berthoz · Guy Cheron · Joseph McIntyre
Received: 2 October 2012 / Accepted: 9 January 2013 / Published online: 9 February 2013 © Springer-Verlag Berlin Heidelberg 2013
Abstract In the present study, we investigated the effect of weightlessness on the ability to perceive and remember self-motion when passing through virtual 3D tunnels that curve in different direction (up, down, left, right). We asked cosmonaut subjects to perform the experiment before, during and after long-duration space flight aboard the International Space Station (ISS), and we manipulated vestibular versus haptic cues by having subjects perform the task either in a rigidly fixed posture with respect to the space station or during free-floating, in weightlessness. Subjects were driven passively at constant speed through the virtual 3D tunnels containing a single turn in the middle of a linear segment, either in pitch or in yaw, in increments of 12.5°. After
C. De Saedeleer (*) · A. Bengoetxea · A. M. Cebolla · G. Cheron Laboratory of Neurophysiology and Biomechanics of Movement, Université Libre de Bruxelles, CP 640, 50 Av F Roosevelt, Brussels, Belgium e-mail:
[email protected] C. De Saedeleer · G. Cheron Laboratory of Electrophysiology, Université de Mons, Mons, Belgium M. Vidal · A. Berthoz Laboratoire de Physiologie de la Perception et de l’Action, LPPA UMR 7152, CNRS Collège de France, 11 place Marcelin Berthelot, 75005 Paris, France M. Lipshits Institute for Information Transmission Problems, Russian Academy of Sciences, Bol’shoi Karetnyi per., 19, 127994 Moscow, Russia J. McIntyre Centre d’Etude de la Sensorimotricité, CESEM UMR 8194, Institut Neuroscience et Cognition, CNRS - Université Paris Descartes, 45 rue des Saints Pères, 75006 Paris, France
exiting each tunnel, subjects were asked to report their perception of the turn’s angular magnitude by adjusting, with a trackball, the angular bend in a rod symbolizing the outside view of the tunnel. We demonstrate that the strong asymmetry between downward and upward pitch turns observed on Earth showed an immediate and significant reduction when free-floating in weightlessness and a delayed reduction when the cosmonauts were firmly in contact with the floor of the station. These effects of weightlessness on the early processing stages (vestibular and optokinetics) that underlie the perception of self-motion did not stem from a change in alertness or any other uncontrolled factor in the ISS, as evidenced by the fact that weightlessness had no effect on the perception of yaw turns. That the effects on the perception of pitch may be partially overcome by haptic cues reflects the fusion of multisensory cues and top-down influences on visual perception. Keywords Weightlessness · Asymmetry · Pitch · Perception
Introduction The ability of humans to perceive and remember self-motion as they navigate through a 2D or 3D environment relies upon the integration of multimodal sensorimotor information, including static or dynamic visual cues, proprioception, vestibular cues, and corollary discharge (Mittelstaedt 1983,1999; Berthoz 1991, Glasauer and Mittelstaedt 1998; Vidal and Bülthoff 2009). It is reasonable to assume that these same sensory cues might contribute to the perception of what the physical environment offers in terms of potential motor actions (Sciutti et al. 2012). Addressing the question of how the CNS integrates spatial information from multiple
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or are any modifications to the perception brought about by the differing affordances and consequences of actions that occur in the unique conditions of weightlessness?”
Methods Figure 1 illustrates the experimental task. Subjects looked straight ahead through a form-fitting face mask and a cylindrical barrel frame at the screen of a laptop computer onto which the images of virtual movements were displayed. The screen was centered on the line of gaze at a distance of ~30 cm from the eyes. The barrel had a diameter of 16.5 cm, yielding a circular field of view subtending 30° in all directions. The form-fitting mask, the barrel, and, if necessary, turning off the lights in the room prevented any external
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sensory cues is fundamental to understanding the workings of the human brain (Pozzo et al. 1998). In this study, we examined the role of gravitational information in the perception of self-motion in 3D. We used a paradigm in which a human subject observed visual stimuli corresponding to what they would see as they moved through a curved tunnel. The tunnel could turn in the horizontal plane to the right or to the left, or it could bend upward or downward in the sagittal plane. The task for the subject was to indicate the amplitude of the turn, based on the visual information provided. This task is of interest for the study of the macroscopic properties of sensorimotor integration because it requires a succession of processing: (1) temporal integration of the sensory input (spatial updating) during the transit through the tunnel, (2) working memory related to the perceived angle, and (3) retrieval (recall) of this angular information. Previously, such a task revealed a significant asymmetry in pitch-induced perception on Earth. Downward stimuli produced a stronger pitch perception than upward, while leftward and rightward yaw turns were perceived equally (Vidal et al. 2006). This up-down asymmetry was also observed when subjects observed a static image of the tunnel (Vidal et al. 2006) and is similar to asymmetrical estimates of the slope of a hillside viewed either from above or from below (Proffitt et al. 1995). To address the question of what reference frames are used to carry out the task, Vidal et al. (2006) recorded responses from human subjects who performed the tasks on Earth in either an upright, seated posture or while lying on their side. In doing so, the investigators decoupled the local, egocentric reference frame defined by the subject’s body from the external, Earth-fixed reference frame defined by gravity and somatosensory cues from the environment. They showed that (1) the up-down pitch asymmetry could arise in either reference frame, (2) asymmetries in OKN responses and the orientation with respect to gravity interacted to determine the response, and (3) the affordances offered by the visual scene could also interact with the sensory cues themselves to determine the perceived angle, depending on the orientation of the body with respect to gravity. In the experiments reported here, we extended this study by testing the effects of gravity, or lack thereof, on the perception of the angle of the turn. We asked cosmonaut subjects to perform the experiment before, during and after long-duration space flight, and we manipulated vestibular versus haptic cues by having subjects perform the task in weightlessness, either in a rigidly fixed posture with respect to the space station or during free-floating. We addressed two specific questions with these experiments, that is, “Does the lack of gravity or graviceptor input alter the sensory processing underlying the perception of self-motion?” and, if so, “Is it the lack of sensory signal per se that causes the disruption,
Exp Brain Res (2013) 226:95–106
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Fig. 1 Simulation of passive self-motion inside a tunnel with a bend in an upward or downward (a–c) and leftward or rightward (b–d) direction. a, b Response indicator in the form of a schematic outside view of the tube, viewed from the side for pitch (a) and from the top for yaw (b); c, d entry (1), bend (2), and exit (3) images for turn angle of 25° for pitch (c) and for yaw (d)
Exp Brain Res (2013) 226:95–106
visual distractions and removed all external visual references (Cheron et al. 2006). Subjects observed on the laptop screen a visual flow corresponding to simulation of passive self-motion inside tunnels in the form of a pipe of constant circular cross section, with stone-textured walls. Each tunnel contained an initial linear segment, a single turn in the middle, either in pitch or in yaw (Fig. 1), with one of 6 possible turn angles ranging from 25° to 87.5° in increments of 12.5° and a final linear segment. Subjects were driven passively at constant speed through the virtual 3D tunnel structure. Images were nonstereoscopic but included perspective cues generated by the OpenGL graphics libraries. Using a typical subject height of 1.75 m as a reference, the visual flow corresponded to a virtual speed of 2.21 m/s (around 8 km/h), corresponding to a fast walking speed for humans. (Additional comments on the realism of the virtual motion can be found in Vidal et al. 2003). After exiting each tunnel, subjects were asked to report their perception of the turn’s angular magnitude by adjusting a response indicator depicting an outside view of a tube on the laptop screen that could be bent by manipulating a trackball. The tube was viewed from the side for pitch turns and from the top for yaw turns (Fig. 1a, b). The tube was initially presented at 0° (corresponding to a straight tunnel), and the subjects were instructed to bend the tube to the perceived turn amplitude by rolling the trackball. They pressed a button to indicate when they had reproduced the deviation angle corresponding to the angle perceived during the simulated movement. After a pause of 5 s, subjects could initiate the subsequent trial with the push of a button. An experimental session consisted of 48 trials, divided into four uninterrupted blocks of 12 trials. A given block included either exclusively pitch turns or exclusively yaw turns. All subjects began with a block of pitch turns, and then alternated, for a block sequence of pitch-yaw-pitchyaw. Each of the 6 possible amplitudes and two possible directions (leftward and rightward for yaw and upward or downward for pitch) occurred just once and in a random order in each block. At the end of a block, feedback about the subject’s performance was displayed before a short pause. This feedback was the error (in degrees) measured between the real turn angle and the reported response, averaged over all trials in the block. Through this score, subjects were made aware of overall performance but received no information about what specific errors were committed. The experiment was preceded by four practice trials: two trials with pitch turns and two trials with yaw turns. During these trials, subjects learned how to use the computer interface, but received no feedback about performance. The full experiment lasted approximately 50 min for a complete session, which included the instructions and practice trials. On Earth, subjects performed the experiment while sitting on a chair of adjustable height facing the computer/
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barrel/mask that was placed on a table. During space flight, cosmonauts performed the experiment in two conditions. In the attached condition, cosmonauts used belts, foot straps, and a tabletop to maintain a sitting like posture in front of the laptop, like the one used on Earth. In the free-floating condition, subjects held the experimental apparatus (laptop computer and tunnel) in their hands with an elastic band holding the mask against the face. An assisting cosmonaut then positioned the subject in the center of the free working volume within one of the space station modules. The subject was released, and both subject and apparatus floated free from any contact with the station. The assisting cosmonaut ensured that no contact with the walls of the station occurred. To accomplish this, the assistant applied short tugs on the clothing of the subject to adjust the position trying to avoid giving strong directional cues. Very few such corrections (1–2 per session per subject) were required. Figure 2 shows the testing schedule for the cosmonauts. Each cosmonaut was tested on 5 successive periods. Prior to flight, cosmonauts were tested on Earth in 2 pairs of sessions over the 2 months preceding liftoff (BF1, BF2). The two sessions within each period were separated by at least 1 day. These subjects were then tested on 2 days over the course of their spaceflight aboard the ISS, with at least 1 day between sessions. Additionally, subjects performed the experiment twice on each day of testing on orbit, once in each of the two different experimental conditions (“attached” (A) and “freefloating” (FF)). The order of passage for the two postural conditions was counterbalanced across subjects. After their return from ISS, cosmonauts were tested on Earth again, on two different days during the week immediately following the landing (PF1) and two more times 1–3 weeks later (PF2). Seven male cosmonauts (C1–C7) participated in this investigation. The mean age (±SD) of the cosmonauts was 42 ± 3 years. Six cosmonauts had previous experience in space flight; one cosmonaut (C2) had no such experience. All cosmonauts were in excellent health, as regularly determined by a special space flight medical commission during all periods of the investigation. Six out of 7 cosmonauts performed the two sessions within the first week of arriving on orbit (not before flight day 2 and not after flight day 7), and the seventh performed the experiment on flight days 16 and 18. The duration of exposure to weightlessness varied between subjects; four of whom spent 10 days on orbit (Russian–Belgian (ODISSEA) and Russian–Spanish (CERVANTES) “taxi” missions), while the other 3 cosmonauts spent 6 months aboard the ISS (Increments 9, 10, and 11). Ten naive subjects (6 men and 4 women), 34 ± 8 years also participated in this experiment; most were students or laboratory staff, and all were right handed. These control subjects performed experimental sessions on the ground following the same schedule as cosmonauts. All participants gave prior written consent before starting this investigation.
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Fig. 2 Timeline of testing performed by each cosmonaut. The experiment was performed at different periods: 2 before, 1 during and 2 after flight aboard the ISS. Within each period, subjects were tested on two separate days, with at least 1 day in between. On each test day, subjects performed a total of 48 trials separated into 4 blocks of 12 trials each. Within each block, trials were all in pitch (up or
down) or in yaw (left or right), and the order of trials was the same for each session (pitch-yaw-pitch-yaw). On each test day on board the ISS, subjects performed two sessions, one in an attached posture and one in free-floating. The order of these sessions on board the ISS was counterbalanced across subjects, with 3 performing attached first and 4 performing free-floating first
Data analysis
angles. We tested whether any changes in perception could be directly attributed to the lack of gravity by comparing the small-angle up/down asymmetry for either free-floating or attached with the ground baselines. We also tested for a direct influence of gravitational cues versus an indirect influence based on haptic cues by comparing the small-angle up/ down asymmetry for the attached versus free-floating posture on orbit.
The perceived turn angle reported by subjects, and the response latencies (corresponding to the time that elapsed between the initial presentation of the response indicator and the moment that the subjects pressed the button to record the response) were recorded for each trial (48 trials/ session), distributed over 4 blocks of 12 trials each. We analyzed primarily the relative angular error as the difference between the real angle and the subject’s response divided by the real angle (see Vidal et al. 2006), signed according to the following convention: positive if the reproduced angle was overestimated (overshot) and negative if it was underestimated (undershot). Analysis of variance (ANOVA) with repeated measures was used to test for statistical significance of the observed response errors. First, we applied separate ANOVA to pitch and yaw data for control subjects and for cosmonauts from their first session on the ground, with direction (up vs. down for pitch, left vs. right for yaw) and turn magnitude (25°, 37.5°, 50°, 62.5°, 75°, or 87.5°) as within-subject factors. Then, based on an observed main effect of turn direction for pitch, but not for yaw turns (see Results), and on previous studies (Vidal et al. 2006), we conducted specific planned comparisons on the computed “up/down asymmetry index” as the average error for pitch downward minus the average error for pitch upward stimuli, as a function of the real turn magnitude and as a function of the experimental session for each subject. Results from pre-flight tests on the ground showed that the up/down asymmetry was limited to the smallest stimulus angles (25°, 37.5°, 50°). We therefore defined the “small-angle up/down asymmetry” as the up/down asymmetry index averaged across these three
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Results Figure 3 illustrates the relative angular error observed for the different real turn magnitudes in control subjects and cosmonauts. Control subjects who performed the experiment on the ground showed a marked asymmetry in the relative angular error for pitch (downward vs. upward) that was strongest for small angles and decreased progressively as the magnitude of the turn increased (Fig. 3a). A two-factor ANOVA revealed a significant main effect of turn direction (F1,9 = 47.2, p
